Microbial Community of Recently Discovered Auka
Total Page：16
File Type：pdf, Size：1020Kb
bioRxiv preprint doi: https://doi.org/10.1101/2021.08.02.454472; this version posted August 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Microbial community of recently discovered Auka vent field sheds light on vent 2 biogeography and evolutionary history of thermophily 3 4 Daan R. Speth1,2 *, Feiqiao B. Yu3,4, Stephanie A. Connon2, Sujung Lim2, John S. Magyar2, 5 Manet E. Peña5, Stephen R. Quake3,4 , and Victoria J. Orphan1,2 6 7 1 Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, 8 CA, USA 9 2 Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, 10 CA, USA 11 3 Department of Bioengineering, Stanford University, Stanford, CA, USA 12 4 Chan Zuckerberg Biohub, San Francisco, CA, USA 13 5 Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, Ensenada, Mexico 14 * Present address: Max Planck Institute for Marine Microbiology, Bremen, Germany 15 16 17 Correspondence: 18 [email protected] or [email protected] 19 20 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.02.454472; this version posted August 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 21 Abstract 22 Hydrothermal vents have been key to our understanding of the limits of life, and the metabolic 23 and phylogenetic diversity of thermophilic organisms. Here we used environmental 24 metagenomics combined with analysis of physico-chemical data and 16S rRNA amplicons to 25 characterize the diversity, temperature optima, and biogeographic distribution of 26 sediment-hosted microorganisms at the recently discovered Auka vents in the Gulf of California, 27 the deepest known hydrothermal vent field in the Pacific Ocean. We recovered 325 28 metagenome assembled genomes (MAGs) representing 54 phyla, over 1/3 of the currently 29 known phylum diversity, showing the microbial community in Auka hydrothermal sediments is 30 highly diverse. Large scale 16S rRNA amplicon screening of 227 sediment samples across the 31 vent field indicates that the MAGs are largely representative of the microbial community. 32 Metabolic reconstruction of a vent-specific, deeply branching clade within the Desulfobacterota 33 (Tharpobacteria) suggests these organisms metabolize sulfur using novel octaheme 34 cytochrome-c proteins related to hydroxylamine oxidoreductase. Community-wide comparison 35 of the average nucleotide identity of the Auka MAGs with MAGs from the Guaymas Basin vent 36 field, found 400 km to the Northwest, revealed a remarkable 20% species-level overlap between 37 vent sites, suggestive of long-distance species transfer and sediment colonization. An adapted 38 version of a recently developed model for predicting optimal growth temperature to the Auka 39 and Guaymas MAGs indicates several of these uncultured microorganisms could grow at 40 temperatures exceeding the currently known upper limit of life. Extending this analysis to 41 reference data shows that thermophily is a trait that has evolved frequently among Bacteria and 42 Archaea. Combined, our results show that Auka vent field offers new perspectives on our 43 understanding of hydrothermal vent microbiology. 44 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.02.454472; this version posted August 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 45 Introduction 46 Microbial communities at hydrothermal vents have long been of interest for their impact on 47 localized productivity and nutrient cycling in the deep ocean, as surface expressions of the 48 subsurface biosphere, and as potential analogs for ocean life on icy moons. These 49 chemosynthetic communities differ strongly from the communities inhabiting the surrounding 50 seafloor, but the variation between different hydrothermal areas is not well understood. Based 51 on host lithology, hydrothermal areas can be classified into three groups: basalt-hosted, 52 ultramafic, and sediment-hosted. The majority of well-studied high temperature vents are 53 basalt-hosted, with hydrothermal fluid directly discharged from fissures into the overlying 54 seawater (Dick 2019). In contrast, sediment-hosted hydrothermal vents such as those found in 55 Guaymas Basin are distinctive for the interaction of the superheated fluid with overlying 56 sediment. This interaction further alters the fluid composition through incorporating 57 thermally-degraded organic compounds during advection to the seafloor, resulting in steep 58 temperature gradients in the sediments and near surface oil production (Procesi et al. 2019). 59 This additional complexity makes sediment-hosted vent fields attractive study sites for microbial 60 ecology (Teske 2020). Indeed, Guaymas Basin has proven to be a particularly rich source for 61 discovery of novel metabolic capabilities of thermophilic microorganisms. Examples include 62 thermophilic anaerobic oxidation of methane coupled to sulfate reduction by consortia of 63 Desulfofervidus sp. bacteria and ANME-1 archaea (Holler et al. 2011; Schouten et al. 2003), 64 anaerobic butane degradation by the sulfate-reducing bacterium Desulfosarcina BuS5 65 (Kniemeyer et al. 2007), and anaerobic butane oxidation by consortia of Synthrophoarchaeum 66 sp. and Desulfofervidus sp. Bacteria (Laso-Pérez et al. 2016). In addition, some of the most 67 extreme hyperthermophiles, Methanopyrus kandleri and Pyrodictium abyssi, with maximum 68 measured growth temperatures of 122ºC and 110ºC, respectively, have been isolated from 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.02.454472; this version posted August 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 69 Guaymas Basin sediments and chimneys (Pley et al. 1991; Kurr et al. 1991; Takai et al. 2008). 70 The outsized role of Guaymas Basin in discovery of microbial processes makes the recent 71 discovery of the Auka vent field, a second sediment hosted hydrothermal vent system along the 72 same fault in the Gulf of California (Goffredi et al. 2017; Paduan et al. 2018; Espinosa-Asuar et 73 al. 2020), especially exciting, as it provides a unique opportunity for comparative analyses of 74 sediment hosted hydrothermal vent systems. 75 Auka is located at >3650m water depth in the Southern Pescadero Basin, a pull-apart basin at 76 the southern tip of the Gulf of California and 400 kilometers southeast of Guaymas Basin. The 77 composition of the hydrothermal fluids at both sites is similar. The fluids are slightly acidic (pH 78 6), with high concentrations of methane (81 / 16 mmol kg-1 ), hydrogen sulfide (10.8 / 6 mmol 79 kg-1 ), and carbon dioxide (49.2 / 43 mmol kg-1 ) at Auka and Guaymas respectively, and 80 comparatively low hydrogen gas concentration (2 mmol kg-1 at Auka) (Von Damm et al. 1985; 81 Welhan 1988; Paduan et al. 2018). The temperature of the fluids measured at chimney orifices 82 is close to 300oC at both locations. Due to these high temperatures, fluids advecting through the 83 sediments at both sites contain thermogenic hydrocarbons, originating from the catagenesis of 84 sediment organic matter. 85 While the similarities between both sites are striking, there are stark differences as well. At 86 3650m Auka is the deepest known hydrothermal vent system in the Pacific